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Amur tiger: a case study of living on the edge

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 McDonald 13-McDonal-chap13 Page Proof page 325 28.8.2009 9:14pm

CHAPTER 13

Amur tiger: a case study of living on the edge

Dale G. Miquelle, John M. Goodrich, Evgeny N. Smirnov, Phillip A.
Stephens, Olga Yu Zaumyslova, Guillame Chapron, Linda Kerley,
Andre A. Murzin, Maurice G. Hornocker, and Howard B. Quigley

# Dale Miquelle AQ1

edge of a species’ distribution provides a lens

Introduction
Although the stereotypic image of tigers usually
places them in a steamy Indian jungle, in fact the
species occupies diverse habitats across a wide range
of latitudes. The Siberian or Amur tiger (Panthera
tigris altaica) is the northernmost, and probably
faces the most severe suite of environmental con-
straints. Although tigers in general have moderate
to low levels of genetic diversity (Wentzel et al.
1999; Luo et al. 2004), and the Amur tiger appears
to be particularly homogenous (Luo et al. 2004; Rus-
sello et al. 2004), its ability to adapt to the hostile
environments of north-east Asia demonstrate the
behavioural and physiological plasticity of this spe-
cies. Understanding how a population survives at the
through which to understand the ecological con-
straints imposed not only on that population but
the species as a whole. Because Amur tigers are al-
ready stressed by extreme environmental conditions,
we should expect them to be more sensitive to
human disturbances. Thus, understanding the im-
pact of humans on tigers at the northern fringe of
their range provides a basis for conserving not only
Amur tigers, but all subspecies.
We hypothesize that the primary constraints on
tiger distribution and abundance are (1) prey distri-
bution and abundance and (2) mortality and habitat
loss caused by people, factors considered critical for
other large felids as well (e.g. Woodroffe [2000], Car-
bone and Gittleman [2002], Dinerstein et al. [2007],
 McDonald 13-McDonal-chap13 Page Proof page 326 28.8.2009 9:14pm

326 Biology and Conversation of Wild Felids

and Hayward et al. [2007]). In this chapter we inves-

tigate how the abundance and distribution of prey
influences density, home-range size, reproductive
parameters, and survival rates of Amur tigers. By
comparing characteristics of Amur tigers with those
of more southern populations, especially Bengal
tigers (Pa. t. tigris), we reveal how varying ecological
constraints influence conservation strategies.
Description of Amur tiger range
The present geographic range of Amur tigers is
primarily confined to the Russian Far East pro-
vinces (Krais) of Primorye and Khabarovsk (Fig.
13.1). There are probably less than 400 adult and
subadult tigers in Russia (Miquelle et al. 2007),
with about 95% occurring in the foothills and

Figure 13.1 (a) Sikhote-Alin and east Manchurian (Changbaishan) mountain ecosystems, and (b) current distribution of
tigers in north-east Asia, based on preferred habitat and track locations from winter surveys in 2005 in the Russian Far East
(Miquelle et al. 2007), and in Northeast China, based on verified reports and surveys in 1998 and 1999 (Jiang 2005; Yu 2005).
 McDonald 13-McDonal-chap13 Page Proof page 327 28.8.2009 9:14pm

Amur tiger: a case study of living on the edge 327

main ranges of the Sikhote-Alin Mountains. There
is also an isolated population of 20 or so tigers
distributed within the East Manchurian (or Chang-
baishan) mountain system of eastern Jilin and
southeastern Heilongjiang Provinces of China and
Southwest Primorski Krai, Russia. Today, most
tigers in the East Manchurian Mountains occur
on the Russian side, but the majority of available
habitat is on the Chinese side. Historically, the
largest tracts and most productive tiger habitat
(and therefore the largest numbers of Amur tigers),
no doubt were found in Northeast China. When
tigers nearly disappeared from the Russian Far East
in the 1940s (Kaplanov 1948; Miquelle et al., in
press), dispersal from China probably contributed
to their recovery in Russia (Heptner and Sludskii
1992). However, the development of Northeast
China, starting in the late nineteenth century and
increasing dramatically in the 1940s, led to habitat
loss and intensive hunting (Ma 2005) so that by
the 1990s the few tigers still reported in Northeast
China were probably mostly dispersers from Russia
(Yu 2005).
In both Sikhote-Alin and East Manchurian forest
ecosystems, peak altitudes are generally 500–800 m
above sea level, few reaching 1000 m or more. Col-
lectively, these two Tiger Conservation Landscapes
(TCLs; Sanderson et al. 2006) represent a zone where
East Asian coniferous–deciduous forests and the bo-
real forests merge, resulting in a mosaic of forest
types that vary with latitude, elevation, topography,
proximity to the Sea of Japan, and past history.
Over 70% of Primorye and southern Khabarovsk is
forest covered and, despite more extensive clearing,
large tracts of forest also remain in Northeast China
(Fig. 13.2). The original dominant forest was com-
posed of a mixture of Korean pine (Pinus koraiensis)
and deciduous tree species including birch (Betula
spp.), basswood (Tilia spp.), aspen (Populus spp.) and
in the north and at higher elevations, conifers such as
spruce (Picea spp.), fir (Abies spp.), and larch (Larix
spp.). Most of these forests have been selectively
logged in the past, and human activities, in associa-
tion with fire, have resulted in conversion of many low
elevation forests to secondary oak (Quercus mongolica)
and birch (Be. costata, Be. lanata, and others) forests. AQ3

Pine and deciduous forests

Conifer and alpiine/tundra

Open meadows, agricultural
fields, and settlements
Northern boundary of pine
and deciduous forests
Historic northern boundary
of tiger distribution
Russian-Chinese boundary

Figure 13.2 Northernmost distribution of tigers, reconstructed from Heptner and Sludski (1992), and distribution of the
mixed-pine (Pinus koraiensis and Pinus sylvestris) broad-leaved and pure deciduous forests, based on data from two sources:
a vegetation map of the Amur Basin developed under V.H. Sochavi (Soviet Academy of Sciences, 1968) and a map of habitat
types of Sikhote-Alin by V.V. Ermoshin, A.A. Murzin, and V.V. Aramilev (Institute of Geography, Far Eastern Branch of the
Russian Academy of Sciences) interpreted from Landsat 5 satellite imagery.
 McDonald 13-McDonal-chap13 Page Proof page 328
328 Biology and Conversation of Wild Felids
We have intensively studied Amur tigers (from
1992 to present) in the Sikhote-Alin Zapovednik (Re-
serve), an IUCN Category I protected area which
straddles the Sikhote-Alin Mountains (Fig. 13.1)
and is the largest protected area containing tigers in
north-east Asia.
The climate in this region is monsoonal, with 75–
85% precipitation (650–800 mm in central Sikhote-
Alin) occurring between April and November. The
January monthly mean temperature is
22.6 C on
the inland side of the central Sikhote-Alin Moun-
tains, but the Sea of Japan moderates temperatures
(and snow depths) on the coastal side of the range,
when the January monthly mean is
12.4 C. The
frost-free period (which influences plant productivi-
ty) varies between 105 and 120 days/year. Snow
depth varies greatly by locale and year, but averages
22.6  2.9 cm in mid-February (60-year mean) in the
inland central Sikhote-Alin and only 13.7  3.5 cm
on the coast (data from Primorye Weather Bureau).
However, heavy snowfalls, most common in March,
can have dramatic impacts on ungulate and tiger
populations.
Food habits and prey preferences
of Amur tigers
By necessity tigers have developed the capacity to
prey on a wide range of species. However, there is
doubtless a suite of species and body weight ranges
that tigers prefer, which likely maximize the differ-
ence between energy expended and gained in acquir-
ing prey, tempered by the risk associated with
capture (Hayward and Kerley 2005). Tigers are likely
to forage optimally when taking the largest prey that
can safely be killed (Pyke et al. 1977; Hayward and
Kerley 2005), often ungulates their own size or larger
(Sunquist and Sunquist 1989). The list of primary
prey across Asia usually includes a suite of large-and
medium-sized cervids, as well as suids and bovids
(Table 13.1).
The ungulate complex of north-east Asia is repre-
sented by seven species, with red deer (Cervus ela-
phus; for body weights see Table 13.2), wild boar
(Sus scrofa), and Siberian roe deer (Capreolus pygargus)
the most common: all are found throughout the
28.8.2009 9:14pm
Sikhote-Alin and much of the eastern Manchurian
Mountains, but are rare in higher altitude spruce–fir
forests. Red deer become rarer in the southern por-
tions of this region, where they are replaced by sika
deer (C. nippon) which reach their northern limits in
central (inland) and northern (along the coast) Pri-
morye. Roe deer are often associated with forest
‘edge’ habitats, but also occur in forests throughout
the region. Manchurian moose (Alces alces came-
loides) (281 kg; Bromley and Kucherenko 1983)
reach the southern limits of their distribution in
central Sikhote-Alin Mountains, and are sparsely
distributed in the inland boreal forests, but more
abundant further north. Musk deer (Moschus moschi-
ferus) are most commonly associated with conifer
forests, but can be found in a wide variety of forest
habitats. Goral (Nemorhaedus caudatus; 32 kg; Vo-
loshina and Myslenkov 1994), a rare wild goat, are
mostly limited to coastal cliff habitat. Unique to
north-east Asia is the absence of wild bovids in the
spectrum of available prey for tigers (Table 13.1).
Although bovids do not always represent a large per-
centage of the items selected, because of their size
they can provide a significant proportion of the total
biomass consumed by tigers (Karanth 1993).
Representing both potential competitors and prey,
brown bear (Ursus arctos) and Asiatic black bear
(U. thibetanus) are common in north-east Asia.
Given a relatively broad range of potential prey, it
is not surprising that Amur tigers have been reported
eating everything from eagles to seals to brown
bears. However, of 720 kills made by tigers found in
and around Sikhote-Alin Zapovednik between 1962
and 2003, 94% were ungulates, with red deer the
primary prey item (54%) followed by wild boar
(28%; Miquelle et al. 2005c). Roe deer accounted for
only 6% of the diet. Sika deer and musk deer ac-
counted for 3% and 1% of the kills, respectively,
while bears (both Himalayan and brown bears)
accounted for <3% of the kills.
Data from six other sites across tiger range in Rus-
sia confirm that red deer and wild boar are the two
key prey species (63–92% of kills, collectively) and
that combined with the two medium-sized cervids
(sika and roe deer), these four ungulates comprise
81–94% of kills (Miquelle et al. 1996). Kill data some-
times under-represent smaller prey items but ana-
lyses of scats in Sikhote-Alin Zapovednik also
Table 13.1 Summary of ungulate assemblages in tiger range.

Huai Kha Taman Sikhote-Alin

Chitwan, Kanha, Nagarahole, Sunderbans, Khaeng, Negara, Zapovednik,
Type Nepala Indiab Indiac Bangladeshd Thailande Malaysiaf Javag Sumatrah Russiai

Large Present Present Present Formerly Present Present Present Present Present
deerj
Medium- Present Present Present Present Formerly Absent Absent Absent Present
sized
deerk
Small Present Present Present Present Present Present Present Present Present
deerl
Wild pigsm Present Present Present Present Present Present Present Present Present
Large Present Present Present Formerly Present Present Present Present Absent
bovidsn
a
Sunquist (1981); b Schaller (1967); c Karanth (1993); d Heindrichs (1975); e Seidensticker (1986); f Kawanishi (2002); g Rabinowitz (1989); h O’Brien et al. (2003) and Seidensticker and
McDonald 13-McDonal-chap13 Page Proof page 329

Suyono (1980); i this book.

j
Large deer-Al. alces, Ce. elaphus, Ce. unicolor, Ce. duvauceli, Ce. schomburgki, and Ce. timorensis
k
Medium-sized deer-Ce. nippon, Ca. capreolus, Axis axis, Ax. porcinus, and Ce. eldii
l
Small deer-Muntiacus spp., Moschus moschiferus, and Tragulus spp.
m
Wild pigs-S. scrofa, S. verrucosus, and S. barbatus
n
28.8.2009 9:14pm

Large bovids-Bos gaurus, Bos frontalis, Bos javanicus, Babulus babulis

 McDonald 13-McDonal-chap13 Page Proof page 330 28.8.2009 9:14pm

330 Biology and Conversation of Wild Felids

Table 13.2 Jacobs’ index as a comparison of preference by tigers for five ungulate species, based on
proportion of kills and proportion of available ungulate prey numbers (from average prey density) for nine 3-year
periods between 1966 and 2002 in Sikhote-Alin Zapovednik, Russia.

Jacobs 95% Proportion of prey Proportion of kills Adult female body

Species index CI numbers (availability) by tigers mass (kg)

Wild 0.749 0.094 0.054 0.292 86.0a

boar
Red 0.263 0.139 0.453 0.589 149b
deer
Sika
0.571 0.295 0.035 0.024 74b
deer
Roe
0.737 0.104 0.341 0.070 35b
deer
Musk
0.862 0.117 0.117 0.013 12c
deer
AQ4 Notes: Jacobs’ index (Jacobs 1974) is estimated as D = (r
p)/(r + p
2rp), where r is the proportion of total kills made up by a species and
p is the proportional availability of the prey species. D ranges from +1 to
1, where +1 indicates maximum preference and
1 maximum
avoidance.
a
Bromley and Kucherenko (1983)
b
Dalnikin (1999)
c
Prikhodko (2003)

confirmed that these four ungulates were the domi-
nant food items (86% of diet items in scat, compared
to 90% of kills), although other prey, including both
species of bears and smaller prey items such as bad-
gers (Meles leucurus), appeared more commonly in
summer scats.
Given their relative size and abundance, as well as
the risks associated with capturing them, we would
predict that red deer and wild boar should be not
only the most common, but also the most preferred
prey items for Amur tigers. To test this, we used kill
data from Sikhote-Alin Zapovednik for the years
1962–72 (from Gromov and Matyushkin [1974])
and 1980–2003 (from Miquelle et al. [1996, 2005c])
to estimate percentage of occurrence of various prey
in the diet, and used yearly surveys of ungulates
based on winter track counts (1966–2003) converted
to numbers (Stephens et al. 2006) to provide an esti-
mate of proportional abundance. We focused on that
portion of the Zapovednik east of the Sikhote-Alin
Divide to estimate prey densities, because that is
where nearly all tiger kills were reported and because
prey densities and proportions vary greatly east and
west of the divide (Stephens et al. 2006). Because of
small sample sizes in some years, we estimated pro-
portions of each species killed during 3-year inter-
vals, and calculated the mean prey abundance for
these same 3-year intervals. Because surveys are con-
ducted in winter when some prey species are not
active (e.g. bears and badgers), we focused on the
five most common prey species: red deer, wild boar,
roe deer, musk deer, and sika deer (moose are virtual-
ly absent within this study area). Jacobs’ index was
used as an index of preference (Hayward and Kerley
2005).
The results (Table 13.2) reveal that red deer and
wild boar, the two largest ungulates, are the most
preferred with the smaller cervids—musk, roe, and
sika deer—clearly not preferred. However, given that
wild boar are smaller than red deer (Table 13.2), it
would be expected, based on body mass alone, that
they would be less preferred, when in fact, the oppo-
site is true (Table 13.2). Although wild boar, with
their sharp tusks, are probably more dangerous to
hunt, they may be easier to stalk than red deer (Yu-
dakov and Nikolaev 1977). Groups of wild boar, with
 McDonald 13-McDonal-chap13 Page Proof page 331
Amur tiger: a case study of living on the edge
heads down and while foraging noisily in the leaf
litter, are much easier to approach than red deer, and
are likely not as fast when attempting escape. This
greater vulnerability may explain their preferred sta-
tus. Roe deer, though common, may be too small to
be worth hunting. Sika deer numbers have expanded
dramatically in the coastal area of Sikhote-Alin Zapo-
vednik, and have largely replaced red deer as the
most common cervid in the southern Sikhote-Alin
Mountains. However, this trend, which may be
related to global climate changes (Zaumyslova
2000) may not be beneficial for tigers. Although
sika deer appear capable of reaching higher densities
than red deer or wild boar (Gaponov 1991; Gaponov
et al. 2006) they are half the size of red deer, and so
tiger-foraging efficiency may decrease where they are
a primary prey. Despite this concern, tiger popula-
tions in southern Sikhote-Alin appear to be surviving
and reproducing despite the changing suite of avail-
able prey (Miquelle et al. 2007).
What limits tiger distribution
to the north?
The historical northern limit of permanent popula-
tions of tigers in Russia (from Heptner and Sludski
[1992]) coincides strikingly (despite imprecise
knowledge of the tiger’s historical range) with the
northern limits of the pine-mixed deciduous forest
complex of the Russian Far East (Fig. 13.2). This
congruence suggests that these forests represent a
proxy for the northern limits of the tigers’ primary
prey: wild boar and red deer (Fig. 13.3a and b). Al-
though clearly neither species is wholly dependent
on these forest complexes (both extend to complete-
ly different forest ecosystems in Europe), their north-
ernmost limits in the Russian Far East extend only
slightly beyond these mixed pine and deciduous for-
ests. Indeed, the zones of highest densities occur,
with a few exceptions for red deer, in the southern-
most regions of the Russian Far East (Fig. 13.3a and
b), wholly within the limits of this forest complex.
Although red deer (and to a lesser extent wild boar)
occur beyond those limits, their densities are likely
too low to sustain a tiger population. Although other
factors such as extreme cold and deep snows likely
28.8.2009 9:14pm
331
play a role in defining the northern limits of tiger
distribution, the coincidence of prey distribution,
habitat types, and tiger distribution suggests clear
linkages. Thus, although individual dispersing tigers
have been reported more than 1000 km north and
west of their historical range (Heptner and Sludski
1992; Kirilyuk and Puzansky 2000), stable popula-
tions are restricted to more southern regions where
more productive forest systems support prey densi-
ties high enough to allow for successful reproduction
to occur (see below).
The clear linkages between habitat types, prey dis-
tributions, and tiger distribution provide insight into
where tigers historically occurred in nearby China
(Fig. 13.2) which coincides well with existing infor-
mation on their former distribution there (Ma 2005;
Yu 2005). This information, in conjunction with
recent data on where suitable habitat still remains,
provides a mechanism for defining potential tiger
recovery zones in Northeast China (Miquelle and
Zhang 2005).
Tiger density and home-range size
in relationship to prey density
In the absence of human disturbance, available prey
biomass is expected to be the primary determinant of
carnivore density (Carbone and Gittleman 2002;
Karanth et al. 2004c), a prediction supported by
many field studies (van Orsdol et al. 1985; Stander
et al. 1997c; Eberhardt and Peterson 1999; Fuller and
Sievert 2001; Hayward et al. 2007).
In Sikhote-Alin Zapovednik, estimates of ungulate
and tiger numbers have been collected annually
since 1966 (Smirnov and Miquelle 1999; Stephens
et al. 2006). Using average female body mass as a
measure of body size in ungulate populations (with
males weighing more, and subadults and young
weighing less), we converted estimates of numbers
of ungulates into total ungulate biomass for the Za-
povednik (excluding moose and goral, which repre-
sent a minor part of the total biomass, and only 1.4%
of the tigers’ diet). A regression analysis revealed a
strong linear relationship between the total available
prey biomass and tiger density (Fig. 13.4). Because
the most preferred prey—wild boar and red deer—are
 McDonald 13-McDonal-chap13 Page Proof page 332 28.8.2009 9:14pm

(a)
Red deer distribution in
Russian Far East
Lower densities
Higher densities
Northern boundry of Korean
pine-mixed deciduous forests
Historical northern boundary
of tiger distribution

China

n
0 500 Kilometers

a
p
a
J
N

f
o
a
e
S
DPR Korea
100 200 300 400 Kilometers

(b)
Wild boar distribution in
Russian Far East
Lower densities
Higher densities
Northern boundary of Korean
pine-mixed deciduous forests
Historical northern boundary
of tiger distribution

China
n

0 500 Kilometers
a
p
a
J

N
f
o
a
e
S

DPR Korea
100 200 300 400 Kilometers

Figure 13.3 Distribution of (a) red deer and (b) wild boar in the Russian Far East (reconstructed from Bromley and
Kucherenko [1983]) in relation to northernmost distribution of tigers and northern limits of the pine-mixed deciduous forest
complex (from Fig. 13.2).
 McDonald 13-McDonal-chap13 Page Proof page 333 28.8.2009 9:14pm

Amur tiger: a case study of living on the edge 333

0.7 (a)
0.6 18
Tigers/100 km2

16

Tiger density (per /100 km2)

0.5
14
0.4
12
0.3
10
0.2
8
0.1 6
0 4
0 100 200 300 400 500 600
Prey biomass (kg/km2) 2
0
Figure 13.4 The relationship between prey biomass 0 1000 2000 3000 4000 5000 6000 7000 8000 9000
(kg/km2) and tiger population density (adult tigers/100 Prey biomass (kg/Km2)
km2) in Sikhote-Alin Zapovednik, Russian Far East (Y =
0.0009X + 0.623, r2 = 0.63, and p < 0.0001), based on (b)
data collected from 1966 through 2002. Ungulate 18
estimates are based on winter track counts converted to 16
animal abundance using the Formozov formula (Mirutenko 14

Tigers/100 km2
1986; Stephens et al. 2006), and tiger numbers are 12
based on an expert assessment based on interpretation 10
of relative track size, track age, and distance between 8
tracks (Smirnov and Miquelle 1999; Miquelle et al. 2006). 6
y = 0.003x + 4.2688
4
r 2 = 0.3703
2
also the most abundant, this relationship is similar 0
whether we include all ungulate biomass, or only 0 500 1000 1500 2000 2500 3000 3500
that of the preferred species. Preferred prey biomass (kg/km2)

However, when we compared a greater range of
both tiger and prey densities from 13 sites across
Asia (Miquelle et al. 2005c), a curvilinear relation-
ship was revealed (Fig. 13.5). This Type II functional
response has not been reported for any other large
carnivores, but accords with Karanth et al.’s unre-
stricted model (2004c) of tiger density and prey
numbers (the fact that they used prey numbers,
rather than biomass, does confound the compari-
son, but it seems unlikely that conversion to bio-
mass would dramatically change the relationship).
There are several possible explanations for why
this relationship is not linear. The sample size was
small (n ¼ 13), and methods and accuracy varied.
There may also be errors in estimating prey density,
tiger density, or both. However, the parallel with
Karanth et al.’s finding (2004c), which relied upon
independent data and a more rigorous design, sug-
gests that measurement errors are not the explana-
tion. Alternatively, the curvilinear fit might indicate
over-representation of non-preferred species. To as-
sess this, for 9 of the 13 sites for which it was possi-
ble, we recalculated available biomass for the range
Figure 13.5 The numerical response of tigers (animals/
100 km2) to changes in (a) total prey biomass (Y =
13.683e
1229.52/X) and r2 = 0.53) and (b) preferred prey
biomass (y = 0.003x + 4.2688, r2 = 0.37, and p = 0.08).
(Data from Schaller 1967; Tamang 1982; Thapar 1986;
Karanth 1991; Stoen and Wegge 1996; Smirnov and
Miquelle 1999; Karanth and Nichols 2000; Stephens et al.
2006.) The curvilinear relationship in (a) is represented by a
Michaelis–Menton function of the form Y = aeb/X, where Y is
tiger density, X is prey density, and a and b are constants.
of species between 86 and 550 kg, with the lower
limit representing the weight of female wild boar (a
preferred prey of Amur tigers), and the upper limit
representing the approximate weight of adult female
gaur. The relationship based solely on prey within
what is presumed to be the preferred weight range is
linear (Fig. 13.5b), similar to other large carnivores
(Hayward et al. 2007), but is not strong and margin-
ally non-significant (r2 ¼ 0.37 and p ¼ 0.08). Wheth-
er this relatively weak linear relationship (Fig. 13.5b)
is a result of insufficient data is as yet unclear, but
suggests that a curvilinear relationship (Fig. 13.5a)
 McDonald 13-McDonal-chap13 Page Proof page 334 28.8.2009 9:14pm

334 Biology and Conversation of Wild Felids

600

Tigress home range size (km2)

500 Y = 36,605X 0.8776
r 2 = 0.987
400

300

200

100

0
0 1000 2000 3000 4000 5000 6000 7000 8000
Prey biomass (kg/km2)
Figure 13.6 A hypothetical relationship between prey biomass and home-range size of adult resident female tigers,
Y =aX(b/X), where Y is female home-range size, X is prey biomass, a = 18.41, and b = 205.506. This relationship assumes
that all tiger populations contain territorial females, and there are on average 2.5 individuals per female home range,
including an adult resident female, a third of a male (assuming males cover home ranges of 3 females), 0.7 cubs (e.g.
Amur tigers on average produce 1.4 cubs/year, but only half survive to 12 months), and 0.5 transients per home range.

may be more appropriate for tigers, providing a
tantalizing indication that other factors (perhaps so-
cial regulation, see below) may be influencing tiger
densities when prey biomass is extremely high.
Wherever they have been studied, tigers have de-
monstrated a spacing system in which females de-
fend territories that overlap little with neighbouring
females, and males defend territories that include
one to nine tigresses (Smith et al. 1987; Goodrich
et al. 2005). Females are expected to maintain home
ranges sufficiently large to ensure adequate resources
for rearing young, but as small as possible to avoid
unnecessary defence costs (Smith et al. 1987; Sandell
1989). Consequently, female home-range size is pre-
dicted to be inversely related to prey density (Sandell
1989), but there are too few data to test this for tigers.
However, assuming there are 2.5 animals/female
home range in the average tiger population (assum-
ing, in addition to the adult female, 0.3 adult males–
female home range, 0.7 cubs/year/home range, and
0.5 transients), it is possible to derive a prediction for
female tiger territory size using estimates of prey
biomass and tiger densities from Fig. 13.5a. This
model (Fig. 13.6) provides reasonable estimates
where measurements of home range exist, correctly
predicting 445 km2 for tigresses in Sikhote-Alin Za-
povednik Russia (vs. the actual estimate of 440 km2;
Goodrich et al. 2005) but slightly overestimating
home-range size for Chitwan National Park, Nepal
(41 km2 vs. the actual estimate of 20.7 km2; Smith
et al. 1987). Across the range of tigers in Asia, female
home-range size appears to calibrate so as to provide
a similar prey biomass per home range. Thus, al-
though home-range size of resident female Amur
tigers in Sikhote-Alin Zapovednik is, on average, 22
times larger than that of Bengal tigers in Chitwan,
total prey biomass per female home range is approx-
imately equal (actually 1.2 times greater in Sikhote-
Alin than Chitwan), using data from Tamang (1982)
and Stephens et al. (2006) to calculate prey biomass.
These results suggest that prey density is a driving
force in determining home-range size in female
tigers, as predicted for solitary carnivores (Sandell
1989), and consequently is of major importance in
considering area requirements for viable populations
of tigers. The curvilinear relationship in Fig. 13.6 also
suggests that as prey biomass becomes very large,
there may be a minimum home-range size for adult
females (10–20 km2), below which social regulation
may start to influence tiger densities.
At the other end of the spectrum, Figs 13.4 and
13.5a suggest that tigers in Sikhote-Alin Zapovednik
are close to the lower limits of prey densities at which
tigers can exist. Without the constraints of rearing
 McDonald 13-McDonal-chap13 Page Proof page 335
Amur tiger: a case study of living on the edge
cubs, home ranges can continue to increase to en-
sure sufficient prey can be found, as demonstrated
by male Amur tigers which maintain home ranges
on average in excess of 1000 km2 (Goodrich et al.
2005). We suggest that, at 440 km2, female Amur
tigers within our study area are nearing the limits of
home-range size in which reproduction can suc-
cessfully occur. While prey densities decline further
to the north where tigers still occur (and presum-
ably home ranges increase in size), the logistics of
capturing ample prey in the vicinity of immobile
young cubs, finding sufficient food to feed subadult
cubs still dependent on their mother (amounting
to 2–4 times her individual energetic needs), and
the energetic demands of covering such large areas
may make significantly larger home ranges non-
viable for breeding females.
Reproduction, survival rates,
and population persistence
All northern ungulates demonstrate a birthing pulse
in late spring and early summer that ensures that the
most nutritious forage will be available to females to
compensate for the energetic demands of lactation,
and provides the longest period of quality forage for
growth of neonates before facing the rigors of a north-
ern winter. Surprisingly, Amur tigers do not demon-
strate a similar birthing pulse in spring that might take
advantage of vulnerable young ungulates for feeding
young cubs. In fact, while we have observed tigers
giving birth in all but 2 months of the year, the peak
birthing season is July and August (Fig. 13.7). Cougars
(Puma concolor) in northern environments demon-
strate a very similar pattern (Cougar Management
Guidelines Working Group 2005). The period of great-
est energy demands for female felids raising cubs is
likely not when caring for newborns (even though
there is a high energy cost of lactation over the first
few months), but when females must provide food for
nearly full-grown subadults, which still rely on their
mother, and require as much or more energy (in the
case of male cubs) than she does. Our data suggest that
Amur tiger cubs disperse from their natal home ranges
on average at 19 months, and that they are moving
largely independently of their mother by 18 months
of age (Kerley et al. 2003). This suggests that the most
28.8.2009 9:14pm
335
0.5
Percentage of litters
0.2
0.5
0.1
0.05
0
b
ar
r
ay
l
g
p
ct
c
Ju
Ap
No
De
Ja
Fe
Ju
Au
Se
O
M
M
Figure 13.7 The percentage of 27 Amur tiger litters born
in each month to 13 tigresses in and around Sikhote-Alin
Zapovednik, 1992–2004 (Kerley et al. 2003, 2005).
demanding period for females would be when cubs are
15–18 months old. Male cubs at this time are already
larger than their mothers, but seem to be largely de-
pendent on them for food. For females giving birth in
July or August, the peak demands of feeding a family
would occur between October and February of the
next year. As demonstrated above (Table 13.2), tigers
prefer larger prey, but this preference is likely to be
even stronger for females with large cubs. Small pack-
ets of prey (e.g. newborn ungulates) would not provide
sufficient food to feed a family, even if kills were made
daily: we have observed that females with two to three
yearling cubs can consume adult red deer in 24–36 h.
By late autumn and early winter, calves of the year are
sufficiently large to provide reasonable volumes of
meat, and are still relatively easy to catch. Also, hunt-
ing ungulates is probably easier for felids in winter,
when fresh tracks in snow provide clues to finding
prey (Yudakov and Nikolaev 1987), deep snow can
inhibit escape by prey, and soft snow acts as a muffler
for silent stalking. Thus, the shift in birthing season
from spring and early summer, characteristic of Bengal
tigers (Smith and McDougal 1991; Smith 1993) and
captive Amur tigers (Seal et al. 1987), to late summer
may be a strategy for females to ensure maximum prey
biomass is available for their offspring prior to inde-
pendence and dispersal, when energetic demands of
the family unit are greatest.
Given their hostile environment, it might be ex-
pected that reproduction and survival rates of Amur
tigers would be lower than those in more southerly
populations. However, the scanty available data
 McDonald 13-McDonal-chap13 Page Proof page 336
336 Biology and Conversation of Wild Felids
Table 13.3 Comparison of reproduction parameters of Amur tigers in Sikhote-Alin Zapovednik, Russia (Kerley
et al. 2003), and Bengal tigers in Chitawan National Park, India (Smith and McDougal 1991; Smith 1993)
Bengal tigers
Parameter
n Mean
Age of first reproduction 5 3.5
Interbirth intervala 7 21.6
Litter size at first observationb 49 2.98
Litter size at 1 year 38 2.45
a
For Amur tigers, for litters that survived 2 months; for Bengal tigers, for litters that survived >2 weeks.
b
Age at first observation in Nepal was –3 months, and in Russia averaged 4.1 + 1.3 months.
suggest that most reproductive and survival para-
meters of Amur and Bengal tigers are similar. Age of
first reproduction, interbirth interval, and litter size
at birth (or slightly thereafter) are all similar in Ben-
gal tigers in Chitwan National Park, Nepal, and Amur
tigers in Sikhote-Alin Zapovednik (these being the
only two complete datasets that exist for tigers in
the wild; Table 13.3). The only significant difference
is a nearly 50% reduction in litter size after 1 year in
Russia compared to Nepal. This difference is partially
due to the fact that 43% of cub mortality in our study
was directly or indirectly human-caused (Goodrich
et al. 2008), and such sources of cub mortality were
probably rare in Nepal when studies were conducted.
But this difference may also be associated with great-
er energy demands on female Amur tigers forced to
travel over larger home ranges in search of dispersed
prey and greater vulnerability of cubs to predation
and other mortality factors when mothers are away.
In either case, the difference in cub production ap-
pears to have marginal impact on population growth
rates in model simulations (Karanth and Stith 1999)
and appears to be much less important than adult
female survival rates in determining population per-
sistence (Chapron et al. 2008a).
Two additional key parameters in determining
population persistence in large felid populations ap-
pear to be age of first reproduction and interbirth
interval (Chapron et al. 2008a). These two para-
meters greatly influence potential population
growth rates, and because these parameters are great-
er in tigers than other large solitary felids such as
leopards (Pa. pardus) or cougars, potential growth
rates are lower (Fig. 13.8). Consequently, for tiger
28.8.2009 9:14pm
Amur tigers
95% CI n Mean 95% CI
— 6 3.7 0.6
— 7 21.4 4.4
0.19 22 2.5 1.1
0.25 25 1.3 0.5
populations to persist, survival rates of adult females
must be higher than for these other solitary felids,
and must average over 84% (Fig. 13.8). In this regard,
the only two estimates of survival rates for tigers are
not encouraging: Goodrich et al. (2008) reported
adult female survival rates of 0.81  0.10 over a 12-
year period based on mortalities of radio-collared
animals in Russia, and Karanth et al. (2006) reported
0.77  0.05 survival rates for an entire population of
tigers in Nagarhole National Park, India, using mark-
recapture analyses of camera-trap data. However, as
noted above, the data from Russia included a period
of intense poaching, in the absence of which, female
survival rates were higher than the 84% threshold
suggested by Chapron et al. (2008a) for population
persistence, and the estimate from India includes
emigration (i.e. emigration and death could not be
differentiated) and combined survival rates of tran-
sients and adults of both sexes. Undoubtedly, surviv-
al rates of adult resident females are considerably
higher than the averaged population value in Nagar-
hole. Thus, despite dramatic differences in many
facets of their biology, key demographic parameters
and the constraints on population persistence ap-
pear to be remarkably similar across tiger subspecies
in very different environmental settings.
Conservation implications
Our studies of the northernmost population of tigers
demonstrate the capacity of tigers to adapt to ex-
treme environmental gradients. Variation in prey,
tiger, and human densities as well as human impacts
 McDonald 13-McDonal-chap13 Page Proof page 337
1.5
1.3
Asymptotic growth rate
1.1
0.9
0.7
0.5
0.5 0.6 0.7 0.8
Breeder survivorship
Figure 13.8 Asymptotic growth rates (lambda) of
cougars, leopards, and tigers as a function of adult breeding
female survival rates and species-specific demographic
characteristics (age of first reproduction and interbirth
interval), derived from a branching process model designed
specifically for solitary felids (Chapron et al. 2008a).
are all parameters that influence appropriate conserva-
tion strategies for tigers. Here we consider two key
components of tiger conservation: first, how human
impacts that directly affect mortality influence viabili-
ty of tiger populations, and secondly, how to consider
land-use planning (habitat conservation) for tigers
given the range of conditions under which they live.
These components address what we believe to be the
two key threats to survival of tigers: poaching and
habitat loss. Comparing conservation approaches in
the Indian subcontinent versus north-east Asia is use-
ful in that we consider the two ends of the spectrum of
human–tiger relationships: one (India) where islands
of habitat with tigers are surrounded by a sea of hu-
manity, and the second (Russia) where isolated ‘is-
lands’ of human settlements are surrounded by vast
forested habitats of tigers.
Anthropogenic impacts as mortality
agents
Although little information exists, the vast majority
of tiger mortalities appear to be human-caused
(Schaller 1967; Miquelle et al. 2005a; Goodrich et al.
28.8.2009 9:14pm
Amur tiger: a case study of living on the edge 337
2008). In Russia, the most unbiased estimate indi-
u ga
r cates that 83% of mortalities were human-caused,
Co with poaching the dominant factor (Goodrich et al.
ard 2008). A similar situation probably prevails across
op
Le much of Asia, and direct human-caused mortality is
er likely to be the crucial determinant of the tiger’s
Tig
future. While relatively high mortality rates of cubs
and subadults can be tolerated, mortality rates ex-
ceeding 16% for resident, breeding females is likely
to lead to population declines, and ultimately to
extinction (Chapron et al. 2008a). Age of first repro-
duction and interbirth intervals—variables that ap-
pear to be more or less physiologically and/or
ecologically constrained—are high in comparison
0.9 1.0 to other large felids, and consequently restrict the
tiger’s ability to respond to high mortality rates by
increasing birth rates. These findings are paralleled in
lions, the other large felid of approximately the same
size, which appear to be able to sustain only limited
levels of human-caused mortalities (Whitman et al.
2004). Tiger populations do not appear to be nearly
as ‘resilient’ to human perturbations as has previous-
ly been thought (Sunquist et al. 1999)
Prey recovery efforts are essential for recovery of
tiger populations across much of the remaining suit-
able habitat in Asia (Karanth and Stith 1999; Karanth
et al. 2006), and it is clear that, in the absence of high
rates of human-caused mortality, tiger density is di-
rectly related to prey abundance (Figs 13.4 and 13.5a;
Karanth et al. 2004c). However, because humans are
the primary mortality agent of tigers, reduction of
human-caused mortality is an essential prerequisite
to their conservation. Existing tiger conservation
strategies focusing solely on landscape planning (Mi-
quelle et al. 1999a; Wikramanayake et al. 2004) or
prey recovery (Karanth and Stith 1999) alone may
not be sufficient if mortality rates of adult breeding
females exceed 16%. Despite evidence of some varia-
tion in reproductive success between Amur tigers
and other populations, the key parameters that
limit responses by tigers (age of first reproduction
and interbirth intervals) appear similar across their
range (Table 13.3). The importance of reducing
human-caused mortality on adult females appears
to be universal for tiger populations across Asia.
Localized extinctions of tiger populations in India
(Dinerstein et al. 2007) demonstrate that poaching
can eliminate tiger populations, despite high prey
 McDonald 13-McDonal-chap13 Page Proof page 338
338 Biology and Conversation of Wild Felids
densities and the potential for high tiger densities.
Hence, control of poaching and other sources of
human-caused mortality must be at the forefront of
tiger conservation initiatives across their range.
Habitat loss and fragmentation
Like tigers elsewhere, Amur tigers prey on medium-
sized and large cervids and wild boar, although wild
cattle, an important component of the diet in some
parts of Asia, are absent in the north. Because plant
productivity declines with latitude, carrying capacity
for these preferred prey in northern temperate forests
is reduced by an order of magnitude in comparison
to southern areas. Prey biomass estimates in high-
quality habitats in India range from 2000 to nearly
7500 kg/km2, whereas in the Russian Far East, quality
habitat supports a prey biomass of less than 600 kg/
km2 (Fig. 13.4). Consequently, female Amur tigers
maintain home ranges that are more than 20 times
larger than those of Bengal tigers to find sufficient
food to raise young (Fig. 13.6), and their birthing
season has shifted to increase hunting success
when demands on females with young are greatest.
Given these constraints, tiger densities in the Rus-
sian Far East rarely exceed one animal/100 km2,
whereas some parts of India can boast of more than
16 tigers/100 km2.
The conservation implications of these ecological
differences are vast. Within the Indian subcontinent,
tiger conservation is largely predicated on retaining
viable populations within individual protected areas
(e.g. Thapar [1999]). Such a tactic would be impossi-
ble in the north. At 4000 km2, Sikhote-Alin Zapoved-
nik is the largest protected area in Russia within tiger
range, yet harbours fewer than 30 animals, at least
half of which regularly use areas outside its bound-
aries. A similarly sized reserve in India could contain
640 tigers in an ideal setting. Because Amur tigers
require vast home ranges, no single protected area
can retain a viable population of tigers. Yet protected
areas do provide a haven for tigers and their prey. On
unprotected lands adjacent (and presumably similar)
to zapovedniks, tigers occur at 50% of the densities
observed in zapovedniks because prey densities are
lower and anti-poaching efforts are generally weaker
(Miquelle et al. 2005b). Thus the reserve network acts
28.8.2009 9:14pm
to provide source populations. Therefore, a success-
ful tiger conservation strategy in north-east Asia will
depend upon creating and effectively managing a
core network of protected areas that are connected
to and interspersed with multiple-use lands where
tiger conservation is integrated with sustainable use
of natural resources by humans (Miquelle et al.
1999b, 2005a; Miquelle and Zhang 2005).
Although there are more tigers in India than in any
other country, its burgeoning human population has
fragmented remaining tiger populations into small,
isolated pockets of habitat. The total amount of land
available for tiger conservation is quite similar in
north-east Asia (Russia and Northeast China) and
the Indian subcontinent—271,298 versus 227,569
km2—but in north-east Asia there exist two TCLs
(Sikhote-Alin and east Manchurian mountains) that
average 135,649 km2, while in the Indian subconti-
nent there are 40 TCLs that average only 2100 km2 in
size (Sanderson et al. 2006). Of course, the potential
number of tigers that can be held in these landscapes
is dramatically different. Ranganathan et al. (2008)
suggest that with effective management both inside
protected areas and in adjacent matrices, over 6000
tigers could be retained on the Indian subcontinent,
but in a more likely scenario where adjacent land
matrices are hostile for tigers, only around 3600
tigers would survive (provided protected areas are
well managed). In north-east Asia, tiger densities
could increase if effective ungulate management is
practiced outside protected areas, and poaching is
eliminated within protected areas. However, densi-
ties above 1.0 tigers/100 km2 are likely to occur only
in the most productive habitats, and numbers ex-
ceeding 1000 Amur tigers are unlikely.
At least in the short term, the focus on protected
areas has been successful in retaining tigers in the
Indian landscape, although this strategy is a risky
one, as the probability of extinction for any one of
those isolated populations is relatively high because
survival is dependent upon strong government regu-
lation and compliant people—neither of which is
likely to be continuous. Ranganathan et al. (2008) sug-
gest that survival of tigers in the vast majority of these
landscapes will be dependent on how the environment
surrounding protected areas is managed: under less
favourable conditions in the surrounding areas, the
estimated median population size for 129 of the 150
 McDonald 13-McDonal-chap13 Page Proof page 339
Amur tiger: a case study of living on the edge
protected areas is only 8 tigers. As this seems to be the
scenario developing in India, in the near future, we are
likely to witness many localized extinctions of the kind
experienced in Sariska National Park (Dinerstein et al.
2007). But even with more effective landscape manage-
ment in adjacent territories, which would increase me-
dian population size to 14 (Ranganathan et al. 2008),
the long-term prospects of these small populations is
bleak, as genetic drift and inbreeding depression would
likely become major concerns, and active manipula-
tion of populations would be necessary to retain the
genetic integrity of the Bengal subspecies. Ranga-
nathan et al. (2008) suggest that there are 21 protected
area clusters that are sufficiently large to retain viable
populations of tigers even in a hostile environment,
and it is these areas that are probably the last hope for
tigers in the Indian subcontinent.
In contrast to the Indian subcontinent, tiger habitat
in the Russian Far East is largely unfragmented, al-
though the risk of future fragmentation exists (Carroll
and Miquelle 2006). Nonetheless, despite the fact that
Amur tigers require home ranges exceeding 400 km2,
at approximately 430–500 tigers (Miquelle et al. 2007),
Russia retains what appears to be the largest existent
single population of tigers in the world in a single
unbroken tract of 192,000 km2 of forests, of which
approximately 128,000 km2 (66%) is potential tiger
habitat (Miquelle et al. 1999a). Although future devel-
opment and timber harvest is unavoidable (but can be
managed to reduce impact), a declining human popu-
lation across Russia and specifically an exodus of peo-
ple from the forest villages within tiger habitat provide
hope that this landscape may not undergo serious
fragmentation in the near future.
One similarity that arises from this comparison of
conservation strategies is the urgent need in both
India and north-east Asia to improve management
outside protected areas to increase the effective
amount of habitat for tigers across the greater land-
scape matrix. In India, the task is on the one hand
easier because the scale (total amount of land sur-
rounding protected areas) is much smaller; improved
management on relatively small parcels of land can
greatly increase total population sizes in isolated
TCLs. In Russia, multiple-use scenarios that are com-
28.8.2009 9:14pm
339
patible with tiger conservation must be initiated
across a vast forested landscape, making the task a
more complicated one. However, in India, the de-
mands of a swelling population of 1.1 billion people
make the task there more daunting, while in Russia
the total human population surrounding tiger habi-
tat is less than 2 million, with the vast majority
concentrated in a few cities and peripheral agricul-
tural lands. Hence, the scale of the landscape is vast
in Russia, but the scale of problems associated with
the human population is much greater in India.
In Northeast China, a surprising amount of habitat
still remains (Fig. 13.2), presently largely devoid of
tigers. While more fragmented than nearby Russia,
with a denser human population exerting pressures
on the landscape, there nonetheless still exists the
potential for recovery of tiger numbers in Northeast
China across a broad swath of habitat along the
provincial boundaries of Jilin and Heilongjiang.
This process is underway with the recovery of tigers
in the Hunchun Tiger and Leopard Reserve along the
Sino-Russian border in Jilin Province (Fig. 13.1). Al-
though it will take time, there exists a great opportu-
nity to increase substantially the total population of
Amur tigers, and develop a viable population, sepa-
rate from the existing Sikhote-Alin population, in
the East Manchurian Mountains (Miquelle et al., in
press). Thus, although threats to survival of the Amur
tiger continue to loom, those threats are understood
and rectifiable, if there is sufficient political will and
constraint of human demands on the landscape.
Based on the wealth of legend and lore that has
grown up around the tiger in both Russia and North-
east China, it is clear that not only the natural land-
scape, but also the human landscape will be the
poorer if this population disappears. Yet there is suf-
ficient reason for optimism that this northernmost
representative of Pa. tigris will continue to roam the
forests of north-east Asia, interacting with natural
prey and exposed to the full spectrum of natural
forces that it has survived in for so long, if humans
can provide the minimum requirements of space,
undisturbed habitats, and freedom from direct
human persecution. It is a simple recipe, if we have
the collective societal will to make it happen.
 McDonald 13-McDonal-chap13 Page Proof page 340 28.8.2009 9:14pm

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